Molecular specializations of deep cortical layer analogs in songbirds

Nevue, Alexander A.; Lovell, Peter V.; Wirthlin, Morgan; Mello, Claudio V.

doi:10.1038/s41598-020-75773-4

Cited by 21 publications

(61 citation statements)

References 106 publications

(181 reference statements)

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“…Together with Kv3.1 channels 10,97,120 , this combination of Navα/β subunits narrows the spike half-width and enables fail-safe fastspiking activity to emerge during the critical song learning period. By contrast, juvenile and female 100 RAPNs express high levels of Navβ3, do not have a large I NaR , and cannot spike at high frequencies. Finally, we note a possible evolutionary convergence in firing properties between songbird RAPNs and Betz-type L5PNs in primate motor cortex 9,10 that may have fine-tuned them for rapid and precise motor control 3 .…”

Section: Discussionmentioning

confidence: 89%

“…While it is not known whether these cells express Navβ4 or I NaR , there is evidence that they express high threshold Kv3.1 channels 10 , which are associated with fast-spiking neurons with narrow APs 97,98 . Interestingly, Kv3.1 is notably absent in rodent L5PNs 10 and KCNC1, the gene that encodes Kv3.1, is a strong molecular marker of RA 99,100 . Recently, Navβ4 has been localized to a sparse subpopulation of human L5PNs that project to extratelencephalic areas 101 .…”

Section: Discussionmentioning

confidence: 99%

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Resurgent Na+ currents promote ultrafast spiking in projection neurons that drive fine motor control

et al. 2021

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The underlying mechanisms that promote precise spiking in upper motor neurons controlling fine motor skills are not well understood. Here we report that projection neurons in the adult zebra finch song nucleus RA display robust high-frequency firing, ultra-narrow spike waveforms, superfast Na+ current inactivation kinetics, and large resurgent Na+ currents (INaR). These properties of songbird pallial motor neurons closely resemble those of specialized large pyramidal neurons in mammalian primary motor cortex. They emerge during the early phases of song development in males, but not females, coinciding with a complete switch of Na+ channel subunit expression from Navβ3 to Navβ4. Dynamic clamping and dialysis of Navβ4’s C-terminal peptide into juvenile RA neurons provide evidence that Navβ4, and its associated INaR, promote neuronal excitability. We thus propose that INaR modulates the excitability of upper motor neurons that are required for the execution of fine motor skills.

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Section: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Resurgent Na+ currents promote ultrafast spiking in projection neurons that drive fine motor control

et al. 2021

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“…Molecular analyses, in particular transcriptomic and in situ hybridization methods, have been in-strumental in identifying compelling similarities between the song system and neocortical circuits. In particular, the song motor output nucleus RA (and adjacent regions of the arcopallium in which it is embedded) is transcriptionally similar to layer 5 of the neocortex, where extratelencephalic projection neurons reside [Dugas-Ford et al, 2012;Pfenning et al, 2014;Mello et al, 2019;Nevue et al, 2020]. Likewise, HVC, which projects to various targets in the telencephalon, bears some transcriptional similarity to layer 2/3 of the neocortex, which contains intratelencephalic projection neurons [Pfenning et al, 2014].…”

Section: Birdsong and Its Neural Circuitry As A Window Into Pallial E...mentioning

confidence: 99%

“…Moreover, neural activity in the region that contributes most heavily to OM, the dorsal intermediate arcopallium (AId), is associated with voluntary motor actions, such as hopping and preening [Feenders et al, 2008;Yuan and Bottjer, 2020]. Notably, RA, the arcopallial song motor output nucleus, sits at the medial end of AId and has similar gene expression and connectivity as its neighbor, suggesting that RA is a specialized motor control region derived from ancestral motor circuitry [Feenders et al, 2008;Chakraborty and Jarvis, 2015;Jarvis, 2019;Nevue et al, 2020].…”

Section: Avian Innovation In Pallial Motor Controlmentioning

confidence: 99%

Organizational Conservation and Flexibility in the Evolution of Birdsong and Avian Motor Control

Colquitt

2022

Brain Behav Evol

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Birds and mammals have independently evolved complex behavioral and cognitive capabilities yet have markedly different brain structures. An open question is to what extent, despite these differences in anatomy, birds and mammals have evolved similar neural solutions to complex motor control and at what level of organization these similarities might lie. Courtship song in songbirds, a learned motor skill that is similar to the fine motor skills of many mammals including human speech, provides a powerful system in which to study the links connecting the development and evolution of cells, circuits, and behavior. Until recently, obtaining cellular-resolution views of the specialized neural circuitry that subserves birdsong was impossible due to a lack of molecular tools for songbirds. However, the ongoing revolution in cellular profiling and genomics offers unprecedented opportunities for molecular analysis in organisms that lack a traditional genetic infrastructure but have tractable, well-defined behaviors. Here, I describe recent efforts to understand the evolutionary relationships between birdsong control circuitry and mammalian neocortical circuitry using new approaches to measure gene expression in single cells. These results, combined with foundational work relating avian and mammalian brains at a range of biological levels, present an emerging view that amniote pallium evolution is a story of diverse neural circuit architectures employing conserved neuronal elements within a conserved topological framework. This view suggests that one locus of pallial neural circuit evolution lies at the intersection between the gene regulatory programs that control regional patterning and those that specify functional identity. Beyond birdsong, modifications to this intersection may underlie the evolution of general motor circuitry in the bird pallium and the developmental relationship between these circuits and the avian pallial amygdala.

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“…Thus, it is likely that the electrical synaptic phenotype of cells was acquired in primitive nidopallial and arcopallial networks before the specialization of song motor nuclei. Note that for many other genes, on the contrary, song nucleus-specific gene expression has been documented (http://www.zebrafinchatlas.org/ accessed on 21 August 2021; [36][37][38]). Our results, therefore, suggest that there has been no major evolutionary pressure to modify the cell-type expression pattern of the gene GJD2 in song control nuclei HVC and RA relative to the expression in the regions they evolved from.…”

Section: Electrical Synaptic Phenotype Of Song Nuclei: Evolutionary Considerationsmentioning

confidence: 99%

Extensive GJD2 Expression in the Song Motor Pathway Reveals the Extent of Electrical Synapses in the Songbird Brain

Alcamí

Totagera

Sohnius-Wilhelmi

et al. 2021

Biology

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Birdsong is a precisely timed animal behavior. The connectivity of song premotor neural networks has been proposed to underlie the temporal patterns of neuronal activity that control vo-cal muscle movements during singing. Although the connectivity of premotor nuclei via chemical synapses has been characterized, electrical synapses and their molecular identity remain unex-plored. We show with in situ hybridizations that GJD2 mRNA, coding for the major channel-form-ing electrical synapse protein in mammals, connexin 36, is expressed in the two nuclei that control song production, HVC and RA from canaries and zebra finches. In canaries’ HVC, GJD2 mRNA is extensively expressed in GABAergic and only a fraction of glutamatergic cells. By contrast, in RA, GJD2 mRNA expression is widespread in glutamatergic and GABAergic neurons. Remarkably, GJD2 expression is similar in song nuclei and their respective embedding brain regions, revealing the widespread expression of GJD2 in the avian brain. Inspection of a single-cell sequencing data-base from zebra and Bengalese finches generalizes the distributions of electrical synapses across cell types and song nuclei that we found in HVC and RA from canaries, reveals a differential GJD2 mRNA expression in HVC glutamatergic subtypes and its transient increase along the neurogenic lineage. We propose that songbirds are a suitable model to investigate the contribution of electrical synapses to motor skill learning and production.

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Molecular specializations of deep cortical layer analogs in songbirds

Cited by 21 publications

References 106 publications

Resurgent Na+ currents promote ultrafast spiking in projection neurons that drive fine motor control

Resurgent Na+ currents promote ultrafast spiking in projection neurons that drive fine motor control

Organizational Conservation and Flexibility in the Evolution of Birdsong and Avian Motor Control

Extensive GJD2 Expression in the Song Motor Pathway Reveals the Extent of Electrical Synapses in the Songbird Brain

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